Greenhouse Climate: an Important Consideration when Developing Pest Management Programs for Greenhouse Crops
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1 Greenhouse Climate: an Important Consideration when Developing Pest Management Programs for Greenhouse Crops L. Shipp a Agriculture and Agri-Food Canada Greenhouse and Processing Crops Research Centre Harrow, ON, N0R 1G0 Canada I. Vänninen Agrifood Research Finland MTT Plant Protection Research Jokioinen Finland N. Johansen Bioforsk Plantehelse Norwegian Institute of Agricultural and Environmental Research Hoegskoleveien 7, Ñ-1432 Ås Norway R. Jacobson RJC Ltd. Milnthorpe Garth, Bramham Yorkshire, LS23 6 TH United Kingdom Keywords: biological control, integrated pest management, humidity, lighting, temperature Abstract Greenhouse climate not only has a major impact on plant growth and productivity, but also influences the development, behaviour and interactions among pest and beneficial arthropods present in the greenhouse production system. Studies have demonstrated how temperature and humidity affect the flight activity of pests and their biological control agents. Increased flight activity can increase the dispersal of biocontrol agents and improve the efficacy of pesticide applications. Recent research has shown how seasonal climatic conditions (i.e., temperature, light intensity and photoperiod) affect the parasitism and predation levels of whitefly parasitoids and predatory mites on thrips. In addition, elevated temperatures and low humidity can be used as a control strategy at crop clean up. With the trend to continuous year round production of greenhouse crops, growers in northern temperate climates have started to use supplemental lighting. The effect of continuous or extended lighting on arthropods is not well understood. Also, dynamic temperature regime models are being investigated as an energy conservation method for greenhouse vegetable production. This paper will discuss the current status of our knowledge on how pest dynamics and integrated pest management practices, especially biological control, are influenced by the greenhouse climate. In addition, we will discuss how all year round greenhouse vegetable production under supplemental lighting and how continuous or extended artificial lighting can affect integrated pest management in floriculture and vegetable crops. INTRODUCTION Greenhouse climate (the general spatial above canopy climate and the more specific microclimate within the canopy and around the plant) is a major driving force influencing plant productivity and fruit/flower quality of greenhouse crops (Papadopoulos et al., 1997; van Henten et al., 2006). With the high cost of energy, global warming and the need to protect our environment, energy conservation and energy use efficiency are top priorities of greenhouse growers. Different strategies have been investigated and developed to increase energy conversion, minimize heat loss, and improve energy efficient cooling (Bakker et al., 2008). Growers have also been expanding the production season to essentially year round production where possible to maintain continuity of product supply and increase their competitiveness in the global market share. As a result, this has led to the development of semi- and closed-greenhouse systems to improve control of greenhouse climate variables. However, this technology requires substantial a les.shipp@agr.gc.ca Proc. IS on High Technology for Greenhouse Systems - GreenSys2009 Ed.: M. Dorais Acta Hort. 893, ISHS
2 yield increases to recover the significant financial investment need for structural changes and major changes to the heating, cooling and light systems (Heuvelink and González- Real, 2008). In addition, greenhouse structures are becoming larger and taller, encompassing more area and air volume under one structure. This increases the transmission of light and results in a larger buffer space above the crop for better mixing of air and more optimal and uniform climate conditions for plant production (Jewett and Jarvis, 2001). Insects and mites, just like plants, are impacted directly by greenhouse climate parameters, such as temperature, vapour pressure deficit, CO 2, light intensity and quality and day length. It is commonly known that temperature within the developmental thresholds for arthropods has an inverse relationship to development time (i.e., the higher the temperature the shorter the development period for the arthropod). Beyond that in greenhouses, the impact of climatic variables on arthropod pests and biological control agents is poorly understood compared to plant photosynthesis and productivity. The macroclimate in the greenhouse is easy to measure and record, but it is much more difficult to measure and monitor the microclimate within the plant canopy and on the plant surface. It is in the microclimate sphere where most of the pests and biological control agents are found. At the Greenhouse and Processing Crops Research Centre (GPCRC) we developed a dynamic plant surface climate model (PSCLIMATE- CUCUMBER and PSCLIMATE_TOMATO) for measuring and predicting the microclimate within the canopy and at leaf surface (Zhang et al., 2002; Hao et al., 2008). Being able to predict and manipulate the macro- and microclimate within a greenhouse allows researchers to investigate and better understand the relationship between greenhouse climate and pest outbreaks and at the same time learn how this knowledge can be used to improve management of greenhouse pests. USING GREENHOUSE CLIMATE AT CROP CLEAN-UP IN BETWEEN PLANTINGS FOR PEST CONTROL Manipulation of greenhouse climate parameters such as temperature and humidity are often the most important factors for disease prevention (Jarvis, 1992). An effective clean up or sanitation program at the end of the crop season before the next crop, where economically feasible, will significantly reduce or eliminate pest problems and can delay the onset of future pest infestations until later in the growing season when biological control agents can successfully control the pests. It is well known that the microenvironment can exert substantial influence on the behavior and population dynamics of arthropods (Bursell, 1974a,b; Willmer, 1982). However, little information is documented about how the greenhouse climate can influence pest management strategies for greenhouse pests. Greenhouse crop clean-up trials at the GPCRC, Harrow, Ontario, Canada with cucumber and sweet pepper found that maintaining an average greenhouse temperature and vapour pressure deficit (VPD) at 40 C and 4.76 kpa for 1 day in pepper and 3 days in cucumber resulted in essentially 100% reduction of western flower thrips populations on these crops. The fertigation system to the plants was turned off the day the treatments were started. At 35 C and 3.07 kpa, it was 7-8 days before thrips control reached %. At 30 C and 2.23 kpa, thrips control was inadequate (Shipp and Gillespie, 1993). For greenhouse whitefly on cucumber and tomato, 100% control was achieved after 2-3 days at 40 C and 4.58 kpa and 3 days at 35 C and 3.07 kpa, and % after 5 days at 30 C and 1.05 kpa. For this strategy to be effective, it is important to keep the vents closed and the temperatures constant over a 24-h basis as fluctuating temperatures will result in extended pest survival. However, once temperatures exceed 45 C, greenhouse structures and equipment may be damaged by the heat. MANIPULATING GREENHOUSE CLIMATE TO IMPROVE PESTICIDE EFFICACY Pesticide applications are sometimes the only control option for management of aerial pests such as western flower thrips. It is critical to obtain maximum mortality of the 134
3 pest population with minimal application of the insecticide to avoid the development of pesticide resistance. Insecticide application for thrips is often not very effective because of the habit of thrips preferring dark, closed places, such as the bottom surface of leaves, growing points and flowers, that cannot be reached easily by the applied pesticide. (Powell and Lindquist, 1992). It was hypothesized that the flight activity of adult thrips could be increased by manipulating greenhouse climate conditions resulting in greater exposure of the thrips to the insecticide and subsequently, better control with fewer pesticide applications. Controlled environmental chamber trials in Plexiglas flight boxes found that temperature and VPD significantly affected the flight activity of western flower thrips with 15 C as the low limiting and the combination of 30 C and 2.85 kpa as the high limiting climatic conditions for flight. Greenhouse trials have supported the findings of the controlled environment chamber trials. When an insecticide is used at the end of the crop season, the greatest efficacy can be obtained when temperature and VPD are maintained at 30 C and kpa. When an insecticide is applied during the crop season, a temperature of C and VPD of 0.61 kpa for a 3-h period will increase pesticide efficacy by ca. 25% compared to production conditions of C (Shipp and Zhang, 1999). Flight activity of thrips as indicated by sticky cards placed in the greenhouses during the pesticide treatments showed >200% increase compared to thrips populations collected on sticky cards under normal production climate conditions during spray application. INFLUENCE OF GREENHOUSE CLIMATE ON BIOLOGICAL CONTROL AGENTS/PESTS Efficacy of Entomopathogenic Fungi Beauveria bassiana is one of the most extensively studied entomopathogenic fungi species and is the active agent of many entompathogenic products in use or under development worldwide (Butt et al., 2001; Inglis et al., 2001). Humidity plays a critical role in the germination/sporulation of B. bassiana (Wraight et al., 2000). However, humidity at the top of the canopy may not be the same as humidity within the canopy or microclimate humidity at the leaf surface. At a mean top-canopy air temperature of 23.4 C, humidity was maintained either at 91.6 or 77.1% RH in two cucumber crops at the GPCRC using an overhead misting system. At the middle of the canopy in the high and low humidity greenhouses, humidity decreased to 85.6 and 69.3% RH, respectively. The maximum infection levels for B. bassiana ranged from % and % for the top canopy in the high and low humidity greenhouses, respectively for sprayed adult greenhouse whitefly, western flower thrips and melon aphid (Shipp et al., 2003). The maximum infection level for insect species sprayed in the top canopy was % greater than for the same species sprayed at the middle canopy leaves. The effect of leaf height was higher for adult whiteflies than for melon aphids and western flower thrips. Because of intercepted sunlight, the transpiration of the young leaves is enhanced and humidity at top canopy was 6-8% higher than at middle canopy in both misted and nonmisted greenhouses. In laboratory petri dish trials using filter paper at 75% RH, infection levels for aphids, thrips and whiteflies ranged from %. These results support the existence of a boundary layer of higher humidity around the leaf surface due to transpiration. The microclimate boundary layer at the leaf can vary from mm depending on ambient wind speed, leaf shape and hairiness (Nobel, 1974; Ferro and Southwick, 1984). In greenhouse tomatoes, Boulard et al. (2002) found that the humidity up to 5 mm from the leaf surface was considerably increased compared to ambient humidity when the crop was actively transpiring. Thus, sprayed insects can easily be found within this boundary layer. Biological Control Agent Dispersal According to Chapman (1975), insect flight only occurs under particular conditions, being limited by factors of the external and internal environment and any 135
4 given response may represent an interaction between humidity and temperature. For example, at higher temperatures, such as 30 C and low VPD, insects probably fly to dissipate the extra heat that cannot be dissipated through evaporation when they are at rest. The increased relative air movement when they are in flight promotes convective heat loss and transpiration and subsequently lower body temperature (Bursell, 1974a). At high VPD and the same temperature, the increased flight activity is likely the result of an avoidance response as the insect seeks to find a less desiccating environment. Over a range of temperature and humidity combinations from C and kpa, the predatory bug, Orius insidiosus exhibited no flight activity at 15 C for all VPDs. At 20 and 25 C, flight activity increased with the higher VPDs. Orius insidiosus exposed to 30 C and VPDs 2.04 kpa showed the highest flight activity compared to all other temperature and VPD combinations (Zhang and Shipp, 1998). For O. insidiosus, it was found that the limiting air temperature for flight was humidity dependent. Taking both parameters into consideration a climate index (CI) was determined. Comparing different combinations, CI=T 2 VPD was found to be correlated best with the observed number of flights (r 2 =0.94). The CI threshold for flight activity was determined to be 350 C 2 kpa ½. In a greenhouse cucumber crop, O. insidiosus when released at a canopy height of 1.5 m from a single point source dispersed farther and faster at higher temperatures and VPDs. At 30 C and 2.04 kpa, 98% of the Orius left the release point within 30 min and the distance at which 90% of the recaptured population was found was 6.5 m within 1 h after release and increased to a maximum of 10.4 m after 48 h. At 17.9 C and 0.21 kpa, only 50-60% of the O. insidiosus left the release point after 30 min. The reminder dispersed after 24 h. The maximum distance for the 90 th percentile was 3.90 m after 1 h and was the same after 24 h. If the Orius were released at 1.5 m when top canopy was 2.2 m, the dispersal rate was <25% of what it was when the Orius were released at the top of the canopy. When the O. insidiosus was released below the top of the canopy, temperature and VPD had less influence on flight activity probably due to the interference of the plants and the moderation of the microclimate within the canopy (Zhang and Shipp, 1998). These finding would also be applicable to other aerial predatory bugs or parasitoids. Predation Rate of Predatory Mites and Bugs Predatory mites, such as Neoseiulus cucumeris, are important biological control agents for control of western flower thrips on greenhouse crops. It is known for Phytoseiulus persimilis on two spotted spider mites that higher temperatures cause greater predation rates as a result of the increased energy demand of the predator (Everson, 1980). Stenseth (1979) reported that P. persimilis provided more effective control of spider mites at higher temperatures and humidity (27 C and 70-85% RH). Shipp et al. (1996) found in laboratory trials that VPD influenced the predation rate of N. cucumeris on first instar western flower thrips. A quadratic model was fitted to the predation responses over a VPD range of kpa and the greatest predation rates occurred at either end of the VPD range. However, VPDs at the high end, such as >1.55 kpa are unacceptable for greenhouse production. In greenhouse cage trials on greenhouse cucumber maintained at two leaf temperatures (24 and 20 C) and ambient VPDs of kpa, the predation rate of N. cucumeris was 2 times greater at the higher temperature (8.7 vs. 4.4) (Jones et al., 2005). Sabelis (1986) found that the rate of food resorption from the gut of a mite was directly temperature dependent. Also, at higher temperatures, N. cucumeris is more active than first instar western flower thrips which would probably result in more frequent encounters with its prey. The predation rate did not vary over the range of VPDs. In fact, boundary layer VPD over the leaves was calculated to only range from kpa. Oviposition rate by N. cucumeris also essentially doubled with the higher temperature (2.14 vs eggs per female mite per day). For the predatory bug, O. insidiosus, neither temperature or VPD had an influence on the predation rate of Orius on western flower thrips when presented with 20 first instar larvae over a 24-h period (Jones, 2002). When offered increasing prey densities from first instar thrips, the mean predation rate 136
5 increased from thrips over a 24-h period. Orius was observed to kill more thrips than it could consume, whereas predatory mites will feed on its killed prey before searching for another first instar. Influence of Seasonal Light Intensity, Photoperiod and Temperature on Biological Control Agent Behaviour, Predation and Oviposition Responses In biological control programs, it is important to understand how climatic parameters influence the interaction between the pest and its biological control agent. In greenhouse crop production, climatic parameters are often manipulated to optimize plant growth. These same climate variables also can have a major impact on the pests and biological control agents. Temperature and humidity and their effects on pest-natural enemy interactions have been the most studied climatic parameters (Kajitia, 1983; Nihoul, 1993; Shipp and Gillespie, 1993; Shipp and van Houten, 1997). However, the efficacy of a biological control program often decreases during the winter months even if the control agent is non-diapausing. It has long been recognized that parasitism by Encarsia formosa on greenhouse whitefly is reduced during the winter in northern greenhouses (Parr et al., 1976; Gerling et al., 2001). In addition, augmentative releases of N. cucumeris for control of western flower thrips is less effective in the winter in northern temperate climate regions compared to other times of the year (van Houten et al., 1995). In short term controlled environment experiments Zilahi-Balogh et al. (2006) investigated the influence of light intensity, photoperiod and temperature on the feeding and oviposition activity of two aphelinid parasitoids, E. formosa and Eretmocerus eremicus on greenhouse whitefly. Eretmocerus eremicus parasitized significantly more whitefly hosts than E. formosa in all treatment combinations of light intensity and photoperiod at 24 and 20 C. At 24 C, both parasitoids species parasitized approximately twice as many whitefly hosts at the high light intensity ( W m -2 ) - long day length (L 16:D 8 h) treatment than at the low light intensity (12-14 W m -2 ) - short day length (L 8:D 16 h) treatment. Both E. formosa and E. eremicus parasitized significantly more whiteflies under the simulated summer (i.e., high light intensity [ W m -2 ], long daylength [L 16:D 8 h], 24 C) treatment than the winter (i.e., low light intensity [ W m -2 ], short daylength [L 8:D 16 h], 20 C) treatment. In addition, significantly more dead whitefly hosts were observed in the leaf cages with E. eremicus than E. formosa under the winter treatment, suggesting that Eretmocerus killed more whiteflies through host feeding than Encarsia. This was not the case for the other treatment combinations. Searching behaviour of the two parasitoids, E. formosa and E. eremicus, was then compared under simulated summer [high light intensity (83±1 W/m 2 ), and 24±1 C] and winter [low light intensity (11±0.5 W m -2 ), and 20±1 C] greenhouse conditions on tomato leaflets, with and without a single 3 rd instar greenhouse whitefly host, within a 4-cm tomato leaflet arena (Zilahi-Balogh et al., 2009). Residence time of both parasitoid species was longer on infested leaflets vs. clean leaflets, and longer under winter than summer conditions. When parasitoids encountered a host on infested leaflets, residence time increased. In all cases, residence time of E. formosa was longer than that of E. eremicus. The proportion of time spent searching (i.e., antennating leaf surface while walking or standing still) was longer on clean vs. infested leaflets for both E. formosa and E. eremicus. Walking speed by E. eremicus on clean leaflets was faster than E. formosa under both summer and winter conditions. Host handling time and proportion of host acceptance did not vary among parasitoids. Therefore, E. eremicus is recommended over E. formosa for greenhouse whitefly control for all seasons, especially in the winter when natural light is limiting and where daylight temperatures are 20 C. For predation by N. cucumeris on western flower thrips and its oviposition on greenhouse cucumber under winter vs. summer conditions in a temperate climate, neither light intensity nor photoperiod had an effect on the number of thrips killed by N. cucumeris at 24 C (Zilahi-Balogh et al., 2007). Light intensity, but not photoperiod, had an effect on the number of eggs laid, with more eggs laid at high (83.0±1 W m -2 ) than low 137
6 (11.1±0.5 W m -2 ) light intensity at 24 C. When simulated seasonal light regimes were compared (summer: high light intensity, long daylength vs. winter: low light intensity, short daylength) at the two constant temperatures 20 vs. 24 C, only temperature had an effect. Significantly more thrips were killed at 24 than 20 C irrespective of light regime, which is consistent with light having had no effect in the light intensity photoperiod assay. There was no significant difference in the predation rate on first instar thrips by starved female N. cucumeris during scotophase vs. photophase when raised either under long 16 L:8 D h or short 8 L:16 D h diel cycle. However, N. cucumeris females only laid eggs during the photophase, regardless of the diel cycle in which they were reared. In the winter season, reduced predation by N. cucumeris appears to be influenced more by cooler temperature, than low light intensity and/or short days alone. However, our results also indicate that poor or delayed establishment and numerical response of N. cucumeris in the winter in northern temperate zones in greenhouses under natural light may result from reduced reproductive rate under low light intensity and short daylight conditions. Thus, the use of supplemental lighting should improve biological control of western flower thrips by N. cucumeris in the winter because supplemental lighting will increase oviposition of N. cucumeris due to extended day length and higher light intensities within the crop canopy. This in turn will allow for faster establishment and numerical response by N. cucumeris. In the absence of supplemental lighting, higher release rates of N. cucumeris and/or the addition of an alternative food source (i.e., pollen) during the winter should improve biological control. Also, release methods may need to be reconsidered in wintertime crops. Studies in Finland investigating the establishment of N. cucumeris and A. swirskii in cut roses and gerbera during winter and spring months (January to May) found that the introduction of the predatory mites using slow release sachets did not result in recovery of the mites from the crop until the end of March (I. Vänninen, pers. commun.). Supplemental lighting was used for both crops, but few thrips (prey) were detected in the crops in the N. cucumeris experiment, whereas whiteflies were abundant in the A. swirskii experiment. Thus, photoperiod length was extended in this study, but this did not seem to impact the establishment of the mites. Therefore, just extending the photoperiod length itself may not be enough to influence the reproductive capacity of predatory mites. Light quality needs to be investigated as well as light intensity and photoperiod length. In addition, temperature will also be a major factor to be considered, especially for A. swirskii. Influence of Supplemental Light on Pests and Biological Control Agents With the move to year round production and to increase yield/unit production per m 2, growers are beginning to adopt supplemental lighting in vegetable production and are extending the period of artificial lighting in ornamentals to continuous lighting in the case of rose production. Also, light quality, particularly the ratio between red and far red, has an important influence on plant growth. Thus, plant physiologists are investigating the use of low energy light emitting diode (LED) lights to control the specific wavelengths delivered to the plants. With respect to greenhouse pests, little information is known about how supplemental lighting affects both the pests and their biological control agents. Johansen (2008) reported that continuous lighting (24-h period) in rose production reduced the survival and fecundity of greenhouse whitefly. Egg to adult survival was 45% at continuous lighting compared to 74% at long day (20 L:4 D). Under continuous lighting, 50% of the adult whitefly population laid eggs and the average number of eggs per female during her lifespan was 22. Under long day conditions, 90% of the females laid 53 eggs per female. Preliminary trials with E. formosa indicate that continuous lighting may not affect parasitism rate and survival of the parasitoid. However, Finnish growers report that E. formosa is attracted to high pressure sodium (HPS) lights interfering with their foraging processes. Light quality and intensity can influence the spatial orientation and dispersal of pests (Costa et al., 2002; Mutwiwa et al., 2005; Cloyd et al., 2007; Doukakis and Payne, 2007a,b), host and host plant location (Mellor et al., 1997; Vänninen and Johansen, 2005) and predator fitness (Omkar et al., 2005). In 138
7 addition, light can indirectly affect biological control efficacy through altering the plant s nutritional quality, plant defence mechanisms or the emission of volatile compounds from the plant that insects use for host and host plant location (Nihoul, 1993; Maeda et al., 2000; Vänninen and Johansen, 2005). On the positive side, extending the photoperiod using supplemental light will prevent diapause induction in biological control agents that enter reproductive diapauses under short day lengths. Supplemental lighting will permit the use of the predatory midge, Feltiella acarisuga, Orius spp., Macrolophus spp. and Dicyphus spp. on a year round basis. In Quebec, Canada, the use of supplemental lighting in tomato production permitted the successful establishment of Dicyphus hesperus in the fall and winter and effective control of greenhouse whitefly (Lambert et al., 2005). The use of the supplemental lighting also improved the performance of E. eremicus. Influence of Dynamic Climate Regime on Pests and Biological Control Agents Traditional climate control maintains the greenhouse climate at constant pre-set limits which are assumed to be optimal for plant growth. However, it does not use the natural adaptability of plants to environmental variations to maintain plant productivity. The developmental rates of many crops are determined by long term average temperature rather than instantaneous temperature (De Koning, 1990). The ability of the plant to integrate daily temperature fluctuations within fixed maximum and minimum limits is being used to save energy by using high air temperature during day and low air temperatures at night. Annual heating costs can be reduced by 10% without any yield loss (Van den Berg, 2001). To date, most of the temperature integration research has investigated temperature averaging over 24 h or several days (Rijsdijk and Vogelezang, 2000; Van den Berg, 2001). However, little information is known about how temperature integration affects pests and their biological control agents. In Denmark, growers reported that pest problems decreased when they switched from the traditional to a dynamic climate regime. Jakobsen et al. (2006) found that thrips invasion into greenhouses was linearly correlated to the density of thrips outside the greenhouses, as well as, the amount of vent opening time. Under a dynamic climate regime, the vents were open 6.9% of the time compared to 33.4% under the traditional climate regime over a 25-week period from March to September. Within the greenhouse, the development time of cotton aphid was compared under dynamic vs. traditional climate regime in summer and autumn. The higher summer mean temperature of 24.6 C (dynamic climate) vs C (traditional climate) resulted in a greater number of aphids. During the fall (October to December), the higher mean temperature of 18.8 C (traditional climate) vs C (dynamic climate) did not result in any significant difference in aphid numbers exposed to the two climate regimes (Jakobsen et al., 2005). For biological control agents, Sengonca et al. (1994) found that longevity of Eretmocerus debachi was significantly shorter at fluctuating temperatures (25/35 C, 27/33 C) compared to constant temperature (30 C). When the predation rates of the Orius majusculus on western flower thrips and Coccinella septempunctata on the grain aphid were compared under dynamic (16-30 C and 33-89% RH) and traditional (19-25 C and 36-88% RH) climate regimes, the responses for the two predators were different under the two climate regimes. There was no significant difference in predation rate for C. septempunctata exposed to two climate treatments, whereas, O. majusculus exhibited a higher predation rate under the traditional climate regime. Thus, the impact of the climate regime used in the greenhouse on the biology and control of a pest can vary according to the insect or mite species and needs to be investigated much more thoroughly before any generalizations can be made. INTEGRATED PEST MANAGEMENT IN ALL YEAR ROUND GREENHOUSE VEGETABLE PRODUCTION Consumers worldwide are becoming increasingly sensitive to the potential risks associated with pesticides in food and many are actively seeking produce with no pesticides residues. In the UK, the advanced integrated pest management programs 139
8 already used by growers mean that the risk of pesticide residues being found on homegrown produce is very low. However, there was a gap of three months when there was no greenhouse vegetable production in the UK. Produce was imported from southern Europe where pesticide application was then a normal practice. Thus, the British growers looked for ways to produce all year round (AYR) using supplemental lighting. The first trials were conducted with cucumbers. Two growing systems were compared with supplemental lighting up to 18 h per day depending on natural conditions. A sequence of three crops were grown per year. In the cordon crop training system, the main growing point is removed when the main stem reaches the support wire and lateral shoots are allowed to grow downward. The other system is the new high wire crop training system where a single stem is trained up a vertical string to a 3.6 m horizontal support wire. As the plant approaches the support wire, it is lowered so only the most recent m of growth is vertical. Side shoots and lower leaves are removed so there are no leaves older than 3 weeks on the plant. With the high wire system, thrips, whiteflies and leafhoppers were present on the crop, but population levels remained low. Spider mites were found on the second and third crops and were quickly controlled using P. persimilis. Cotton aphids were found occasionally, but no action was required. The success of the pest management program was attributed to the production practices of frequent leaf removal which likely prevented the pests from completing their life cycles on the plant (Jacobson, 2005). The pests on the crop grown using the cordon system were also kept under control, but the cost of the biological control program was significantly greater than that compared to cordon produced crops without lights. UK growers are now evaluating the high wire system without supplemental lighting. With tomato production under lights, the biological control program was based on Macrolophus caliginosus and interplanting the new crop among the old plants. This way the Marcolophus transferred to the new plants without additional releases of the predatory bug. For leafminer outbreaks, Diglyphus isaea quickly established and provided control. The pollination problem with bumble bees was overcome by releasing the bees when natural lighting became available and closing the hives before natural lighting became limiting. In the UK, there are currently approximately 12 ha of AYR tomato production. The above mentioned integrated pest management program for tomatoes was so successful that the project team received the 2009 UK Grower of the Year Award for Science into Practice (Jacobson, 2008). CONCLUSIONS Greenhouse climate can have a major influence on pest and biological control agent biology and on the control efficacy of not only biological control agents but also other integrated pest management strategies. Greenhouse climate can be used itself as a control strategy at crop clean up. With the switch to more energy efficient production systems such as dynamic climate regimes, continuous lighting in ornamental production and AYR production systems, more research needs to be conducted to determine how these new productions will affect pest population dynamics and existing biological control programs. Literature Cited Bakker, J.C., Adams, S.R., Boulard, T. and Montero, J.I Innovation technologies or an efficient use of energy. Acta Hort. 801: Boulard, T., Mermier, M., Fargues, J., Smits, N., Rougier, M. and Roy, J.C Tomato leaf boundary layer climate: implications for microbiological whitefly control in greenhouses. Agric. Forest Meteorol. 110: Bursell, E. 1974a. Environmental aspects temperature. p In: M. Rockstein (ed.), The Physiology of Insecta, Vol. 2. Academic, New York. Bursell, E 1974b. Environmental aspects humidity. p In: M. Rockstein (ed.), The Physiology of Insecta, Vol. 2. Academic, New York. Butt, T.M., Jackson, C. and Magan, N Introduction: fungal biological controls: 140
9 progress, problems and potential. p.1-8. In: T.M. Butt, C.W. Jackson and N. Magan (eds.), Fungi as Biological Agents: Progress, Problems and Potential. CAB International, New York. Chapman, R.F The Insects: Structure and Functions. The English University Press, London. Cloyd, R.A., Dickinson, A., Larson, R.A. and Marley, K.A Phototaxis of fungus gnat, Bradysia sp. nr. coprophila (Lintner) (Diptera: Sciaridae), adults to different light intensities. HortScience 42: Costa, H.S., Robb, K.L. and Wilen, C.A Field trials measuring the effects of ultraviolet-absorbing greenhouse plastic films on insect populations. J. Econ. Entomol. 95: De Koning, A.N.M Long term temperature integration of tomato: growth and development under alternative temperature regimes. Sci. Hort. 45: Doukas, D. and Payne, C.C. 2007a. Effect UV-blocking films on the dispersal behaviour of Encarsia formosa (Hymenoptera: Aphelinidae). J. Econ. Entomol. 100: Doukas, D. and Payne, C.C. 2007b. Greenhouse whitefly (Homoptera: Aleyrodidae) dispersal under different UV-light environments. J. Econ. Entomol. 100: Everson, P The relative activity and functional response of Phytoseiulus persimilis (Acarina: Phytoseiidae) and Tetranychus urticae (Acarina: Tetranychidae): the effect of temperature. Can. Ent. 112: Ferro, D.N. and Southwick, E.E Microclimate of small arthropods: estimating humidity within the leaf boundary layer. Environ. Entomol. 13: Gerling, D., Alomar, O. and Arno, J Biological control of Bemisia tabaci using predators and parasitoids. Crop Prot. 20: Hao, X., Zhang, Y., Shipp, L. and Borhan, M.S Adaptation and validation of a dynamic plant surface microclimate model (PSCLIMATE) for greenhouse tomatoes. Trans. ASAE 51: Heuvelink, E. and González-Real, M.M Innovation in plant-greenhouse interactions and crop management. Acta Hort. 801: Inglis, G.D., Goettel, M.S., Butt, T.M. and Strasser, H Introduction: fungal biological controls: progress, problems and potential. p In: T.M. Butt, C.W. Jackson and N. Magan (eds.), Fungi as Biological Agents: Progress, Problems and Potential. CAB International, New York. Jacobson, R AYR salad production: the driving forces and potential impact on IPM. IOBC WPRS Bull. 28: Jacobson, R Year-round crop, year-round IPM. HDC News 147: Jakobsen, L., Brogaard, M., Enkegaard, A., Brødsgaard, H.F. and Aaslyng, J.M Dynamic and traditional greenhouse climate regimes: influx of thrips (Thysanoptera). HortScience 41: Jakobsen, L., Brogaard, M., Körner, O., Enkegaard, A. and Aaslyng, J.M The influence of a dynamic climate on pests, diseases and beneficial organisms: recent research. IOBC WPRS Bull. 28: Jarvis, W.R Managing Diseases in Greenhouse Crops. APS Press, St. Paul, MN. Jewett, T.J. and Jarvis, W.R Management of the greenhouse microclimate in relation to disease control: a review. Agronomie 21: Johansen, N.S Influence of continuous lighting on the biology of Trialeurodes vaporariorum (Homoptera: Aleyrodidae). IOBC WPRS Bull. 32: Jones, T.A.P The effectiveness of spinosad and microclimate for use in integrated pest management of thrips on greenhouse cucumbers in Ontario. M.Sc. Thesis, University of Guelph, Guelph, ON, Canada. Jones, T., Shipp, J.L., Scott-Dupree, C.S. and harris, C.R Influence of greenhouse microclimate on Neoseiulus (Amblyseius) cucumeris (Acari: Phytoseiidae) predation on Frankliniella occidentalis (Thysanoptera: Thripidae) and oviposition on greenhouse cucumber. J. Ent. Soc. Ont. 136: Kajita, H Effect of low temperatures on egg maturation and oviposition of 141
10 Encarsia formosa Gahan (Hymenoptera: Aphelinidae) introduced from England into Japan. J. Appl. Entomol. 95: Lambert, L., Chouffot, T., Turcotte, G., Lemieux, M. and Moreau, J Biological control of greenhouse whitefly (Trialeurodes vaporariorum) on interplanted tomato crops with and without supplemental lighting using Dicyphus hesperus (Quebec, Canada). IOBC WPRS Bull. 28: Maeda, T., Takabayashi, J., Yano, S. and Takafuji, A Effects of light on the trotrophic interaction between kidney bean plants, two-spotted spider mites and predatory mites, Amblyseius womersleyi (Acari: Phytoseiidae). Exp. Appl. Acarol. 24: Mellor, H.E., Bellingham, J. and Anderson, M Spectral efficiency of the glasshouse whitefly Trialeurodes vaporariorum and Encarsia formosa its hymenopteran parasitoid. Entomol. Exp. Appl. 83: Mutwiwa, U.N., Borgemeister, C., Von Elsner, B. and Tantau, H.-J Effects of UVabsorbing plastic films on greenhouse whitefly (Homoptera: Aleyrodidae). J. Econ. Entomol. 98: Nihoul, P Controlling glasshouse climate influences the interaction between tomato glandular trichome, spider mite and predatory mite. Crop Prot. 12: Nobel, P.S Introduction to Biophysical Plant Physiology. W.H. Freeman and Company, San Francisco. Omkar, M.G. and Singh, K Effects of different wavelengths of light on the life attributes of two aphidophagous ladybirds (Coleoptera: Coccinellidae). Europ. J. Entomol. 102: Papadopoulos, A.P., Pararajasingham, S., Shipp, J.L., Jarvis, W.R. and Jewett, T.J Integrated management of greenhouse vegetable crops. Hortic. Rev. 21:1-39. Parr, W.J., Gould, H.J., Jessop, N.H. and Ludlam, F.A.B Progress towards a biological control programme for glasshouse whitefly (Trialeurodes vaporariorum) on tomatoes. Ann. Appl. Bio. 83: Powell, C.C. and Lindquist, R.K Ball pest and disease manual. Ball, Geneva, IL. Rijsdijk, A.A. and Vogelezang, J.V.M Temperature integration on a 24-hour base: a more efficient climate control strategy. Acta Hort. 378: Sabelis, M.W The functional response of predatory mites to the density of twospotted spider mites. p In: J.A.J. Metz and O. Diekmann (eds.), The Dynamics of Physiological Structured Populations. Springer-Verlag, Berlin. Sengonca, C., Uygun, N., Ulusoy, M.R. and Kersting, U Laboratory studies on biology and ecology of Eretmocerus debachi Rose and Rosen (Hym.: Aphelinidae), the parasitoid of Parabemisia myricae (Kuwana) (Hom.: Aleyrodiae). J. Appl. Entomol. 118: Shipp, J.L. and Gillespie, T.J Influence of temperature and water vapour pressure deficit on survival of Frankliniella occidentalis (Thysanoptera: Thripidae). Environ. Entomol. 22: Shipp, J.L. and van Houten, Y.M Effects of temperature and vapor pressure deficit on the survival of the predatory mite Amblyseius cucumeris (Acari: Phytoseiidae). Environ. Entomol. 26: Shipp, J.L., Ward, K.I. and Gillespie, T.J Influence of temperature and vapour pressure deficit on the rate of predation by the predatory mite, Amblyseius cucumeris, on Frankliniella occidentalis. Ent. Exp. Appl. 78: Shipp, J.L. and Zhang, Y Using greenhouse microclimate to improve the efficacy of insecticide application for Frankliniella occidentalis (Thysanoptera: Thripidae). J. Econ. Entomol. 92: Shipp, J.L., Zhang, Y., Hunt, D.W.A. and Ferguson, G Influence of humidity and greenhouse microclimate on the efficacy of Beauveria bassiana (Balsamo) for control of greenhouse arthropod pests. Environ. Entomol. 32: Stenseth, C Effect of temperature and humidity on the development of Phytoseiulus persimilis and its ability to regulate populations of Tetranychus urticae 142
11 (Acarina: Phytoseiidae, Tetranychidae). Entomophaga 24: Vänninen, I. and Johansen, N.S Artificial lighting (AL) and IPM in greenhouses. IOBC WPRS Bull. 28: Van den Berg, G.A., Butwalda, F. and Rijpsma, E.C Practical demonstration of multi-day temperature integration. Applied Plant research, Wageningen UR, p.501. Van Henten, E.F., Bakker, J.C., Marcelis, L.F.M., van t Ooster, A., Dekker, E., Stanghellini, C., Vanthoor, B., Van Randeraat, B. and Westra, J The adaptive greenhouse - an integrated systems approach to developing protected cultivation systems. Acta Hort. 718: Van Houten, Y.M., van Rijn, P.C.J., Tanigoshi, L.K., van Stratum, P. and Bruin, J Pre-selection of predatory mites to improve year-round biological control of western flower thrips in greenhouse crops. Entomol. Exp. Appl. 74: Willmer, P.G Microclimate and environmental physiology of insects. Adv. Insect Physiol. 16:1-57. Wraight, S.P., Carruthers, R.I., Jaronski, S.T., Bradley, C.A., Garza, C.J. and Galaini- Wraight, S Evaluation of the entomopathogenic fungi Beauveria bassiana and Paecilomyces fumosoroseus for microbial control of the silverleaf whitefly, Bemisia argentifolii. Biol. Control 17: Zhang, Y., Jewett, T.J. and Shipp, J.L A dynamic model to estimate in-canopy and leaf-surface microclimate of greenhouse cucumber crops. Trans. ASAE 45: Zhang, Y. and Shipp, J.L Effect of temperature and vapour pressure deficit on the flight activity of Orius insidiosus (Hemiptera: Anthocoridae). Environ. Entomol. 27: Zilahi-Balogh, G.M.G., Shipp, J.L., Cloutier, C. and Brodeur, J Influence of light intensity, photoperiod, and temperature on the efficacy of two aphelinid parasitoids of the greenhouse whitefly. Environ. Entomol. 35: Zilahi-Balogh, G.M.G., Shipp, J.L., Cloutier, C. and Brodeur, J Predation by Neoseiulus cucumeris on western flower thrips, and its oviposition on greenhouse cucumber under winter vs. summer conditions in a temperate climate. Biol. Control 40: Zilahi-Balogh, G.M.G., Shipp, J.L., Cloutier, C. and Brodeur, J Comparison of searching behavior of two aphelinid parasitoids of the greenhouse whitefly, Trialeurodes vaporariorum under summer vs. winter conditions in a temperate climate. J. Insect Behav. 22:
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